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Genome-Wide Identification and Characterization of Apple P3A-Type Atpase Genes, with Implications for Alkaline Stress Responses

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Article Genome-Wide Identification and Characterization of Apple P3A-Type ATPase Genes, with Implications for Alkaline Stress Responses Baiquan Ma y , Meng Gao y, Lihua Zhang, Haiyan Zhao, Lingcheng Zhu, Jing Su, Cuiying Li, Mingjun Li , Fengwang Ma * and Yangyang Yuan * State Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A&F University, Yangling 712100, China; [email protected] (B.M.); [email protected] (M.G.); [email protected] (L.Z.); [email protected] (H.Z.); [email protected] (L.Z.); [email protected] (J.S.); [email protected] (C.L.); [email protected] (M.L.) * Correspondence: [email protected] (F.M.); [email protected] (Y.Y.); Tel.: +86-029-8708-2648 (F.M.) These authors contributed equally to this work. y Received: 4 January 2020; Accepted: 5 March 2020; Published: 6 March 2020 Abstract: The P3A-type ATPases play crucial roles in various physiological processes via the generation + of a transmembrane H gradient (DpH). However, the P3A-type ATPase superfamily in apple remains relatively uncharacterized. In this study, 15 apple P3A-type ATPase genes were identified based on the new GDDH13 draft genome sequence. The exon-intron organization of these genes, the physical and chemical properties, and conserved motifs of the encoded enzymes were investigated. Analyses of the chromosome localization and ! values of the apple P3A-type ATPase genes revealed the duplicated genes were influenced by purifying selection pressure. Six clades and frequent old duplication events were detected. Moreover, the significance of differences in the evolutionary rates of the P3A-type ATPase genes were revealed. An expression analysis indicated that all of the P3A-type ATPase genes were specifically expressed in more than one tissue. The expression of one P3A-type ATPase gene (MD15G1108400) was significantly upregulated in response to alkaline stress. Furthermore, a subcellular localization assay indicated that MD15G1108400 is targeted to the plasma membrane. These results imply that MD15G1108400 may be involved in responses to alkaline stress. Our data provide insights into the molecular characteristics and evolutionary patterns of the apple P3A-type ATPase gene family and provide a theoretical foundation for future in-depth functional characterizations of P3A-type ATPase genes under alkaline conditions. Keywords: Apple; P3A-type ATPase; evolutionary pattern; expression pattern; subcellular localization; alkaline stress 1. Introduction Apple (Malus domestica Borkh.) is one of the most important fruit crops and is primarily × cultivated in arid and semiarid regions worldwide [1–3]. The stress conditions of salt-alkalinized soil are a major limitation to crop production worldwide. According to the statistical analysis by the Food and Agriculture organization (FAO) in 2005, about 830 million hectares of the land throughout the world are affected by salt, over half of which (434 million hectares) are alkaline [4,5]. In China, the characteristics of the northwestern Loess Plateau, which include abundant sunlight, deep soils, and considerable daily temperature variations, make it an ideal region for cultivating apple varieties. However, decreases in rainfall and increases in evaporation have resulted in the salinization and alkalinization of the soil in this region. These changes are detrimental for apple tree growth [1]. Forests 2020, 11, 292; doi:10.3390/f11030292 www.mdpi.com/journal/forests Forests 2020, 11, 292 2 of 18 Therefore, selecting the optimal apple rootstock that is resistant to salt–alkaline stress is an important goal for apple breeding programs and apple producers. The salinization and alkalinization of soil are the major global environmental and land resource issues [4,5]. In general, the salinization and alkalinization of soil frequently co-occurring and plant damages induced by the alkalinization (high pH) of soil due to excess NaHCO3 or Na2CO3 are greater than those caused by neutral salts such as NaCl or Na2SO4 [6–8]. Salinity stress can seriously influence plant growth. Several studies have revealed that the overexpression of a gene encoding a P-type H+-ATPase lacking the autoinhibitory domain can increase the salt tolerance of plants [9]. Subsequent studies confirmed that the abundance of P-type H+-ATPases changes in salt-stressed plants [10,11]. Moreover, the posttranslational regulation of P-type H+-ATPase activity is essential for the salt tolerance of halophytic species [12]. High pH stress (alkalinization) causes more severe damage on plants by causing root cell injury and death and then leads to the whole plant wilting and even dying. In plants grown in alkaline soil, a deficiency in PKS5 (salt overly sensitive 2-like protein kinase 5) reportedly increases the tolerance to alkaline stress. Moreover, PKS5 can phosphorylate Ser-931 of P-type H+-ATPases, thereby inhibiting the enzymatic activity [13]. The P-type H+-ATPases activity remains a relatively low level without any stress and increases under saline-alkali stress [14]. In Arabidopsis, the P-type H+-ATPase AHA2 can be regulated by the Ca2+ Sensor SCaBP3/CBL7 and then alkali tolerance is increased [15]. In apple, the P-type H+-ATPases play a key component in + regulation rhizosphere acidification [16]. Overall, P-type H -ATPase (P3A-type ATPase) genes are crucial for plant responses to salt–alkaline stress. Genes encoding P-type ATPases are widely distributed and indispensable in most plant species, in which they are involved in transporting diverse small cations and phospholipids [17,18]. The “P-type” in the name of these enzymes is derived from “phosphorylated intermediate” [19–21]. The P-type ATPases consist of only one catalytic subunit, with considerable domain motions during transport. The structural characterization of plant P-type ATPases has revealed the presence of 8–12 transmembrane domains (TMDs), with the C and N termini of these enzymes exposed to the cytoplasm, as well as the phosphorylation and ATP-binding sites [22]. The P-type ATPase gene superfamily is one of the largest plant gene families [21,23]. These genes were divided into five major families (P1, P2, P3, P4, and P5) with subfamilies (P1B,P2A,P2B,P3A, and P3B) based on the sequence identity and ion specificity [24]. For instance, all of the heavy metal pumps that share significant sequence similarities are classified into + 2+ the P1B subfamily; P1A-ATPase represents the part of the bacterial K transport system; Ca pumps + + + + belong to the P2A-ATPases and P2B-ATPases, Na (H )/K pumps in animals and Na pumps in fungi + are considered as P2C-ATPases and P2D-ATPases, respectively. The plasma membrane H -ATPases, which mediate ATP-dependent H+ transport across the plasma membrane or tonoplast, are classified in the P3 family, P4-ATPases are considered as putative lipid flippases [21,22,25]. The P1B-ATPase transporters such as ATP7A and ATP7B (involved in the regulation of cytoplasmic copper homeostasis via pumping copper into the endomembrane system or out of cell) and mutation of these two genes cause neuropsychiatric disorders such as Menkes and Wilson disease [26]. The P3 family comprises two main subfamilies, namely P3A-type and P3B-type [27,28]. The P3A-type ATPase genes normally encode proton pumps that are located in the plasma membrane, where they mediate the transport of H+ across the plasma membrane and play crucial role in acidification of the aqueous fraction of the cell wall apoplast. In contrast, Ma10 belongs to the P3A-type ATPase gene family, but the encoded enzyme is localized to the tonoplast, where it promotes the vacuolar acidification of apple fruit [29]. Moreover, PhPH1, which encodes a P-type ATPase belonging to the 3B subfamily in petunia, was believed to comprise only bacterial Mg2+ transporters [30]. Furthermore, PhPH1 is present in the tonoplast and cannot transport H+ independently, but it enhances the H+ transport activity in petunia via its interaction with PhPH5 [28]. Gene duplication and selection are two of the major driving forces of morphogenetic evolution. The duplicated genes are nonfunctional or they evolve novel functions (neofunctionalization) or undergo functional differentiation (subfunctionalization) [2,3,31]. During evolution and domestication, Forests 2020, 11, 292 3 of 18 a large proportion of the duplicated genes become nonfunctional because they accumulate deleterious mutations, whereas other duplicated genes undergo neofunctionalization; they are eventually preserved under positive selection pressure [31,32]. Apple, which is a member of the genus Malus in the family Rosaceae, has undergone one autopolyploidization event during its evolution [33,34]. Additionally, a whole genome duplication (WGD) during apple domestication increased the number of chromosomes from nine to seventeen. The duplicated genes arising from the WGD as well as random duplications and segmental duplications exhibited expressional and functional divergence [35]. Thus, deciphering the evolutionary divergence of duplicated apple genes should be investigated during the speciation process. In this study, the P3A-type ATPase gene family was analyzed using the doubled haploid GDDH13 draft genome [32]. Fifteen P3A-type ATPase genes were identified, and the physical and chemical properties of the encoded enzymes were determined. The chromosomal localization, gene structure, gene loss and duplication, and evolution of the P3A-type ATPase genes were also investigated. Additionally,
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